High outcrossing rates and short-distance pollination in a species restricted to granitic inselbergs*
Karina Vanessa Hmeljevski A , Marina Wolowski B , Rafaela Campostrini Forzza A and Leandro Freitas A C
+ Author Affiliations
- Author Affiliations
A Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão 915, 22460-030. Rio de Janeiro, RJ, Brazil.
B Universidade Federal de Alfenas, Rua Gabriel Monteiro da Silva, 700, 37130-001. Alfenas, MG, Brazil.
C Corresponding author. Email: lfreitas.jbot@gmail.com
Australian Journal of Botany 65(4) 315-326 https://doi.org/10.1071/BT16232
Submitted: 13 November 2016 Accepted: 27 April 2017 Published: 22 June 2017
Abstract
Plant populations that are spatially isolated may experience genetic isolation if gene flow via pollination or seed dispersal is limited. The high genetic differentiation among populations of Encholirium horridum L.B.Sm. indicates low gene flow for this species that occurs exclusively on granitic inselbergs in South-east Brazil. Here we describe reproductive and pollination attributes of this bromeliad assessing how they influence the current degree of genetic isolation among populations. The mating system, estimated using five microsatellites markers, indicated allogamy and low pollen pool structure. The breeding system assessed by hand-pollination treatments supported partial self-incompatibility combined with inbreeding depression. Flowers of E. horridum are bell-shaped with crepuscular/nocturnal anthesis, and high nectar production, suggesting chiropterophily. Its pollination system was actually generalist but bats and hummingbirds were more frequent than hawkmoths and crepuscular bees. The high local abundance and large floral display per individual plant contributed to short distance pattern of pollen movement by pollinators. At the intra-population level, this pollinator foraging pattern, with inbreeding depression, promotes low seed viability and individual variations on outcrossing rate. At the inter-population level, those features led to low gene flow. Overall, heterozygosity, maintained by self-incompatibility and inbreeding depression, and pollination by vertebrates described here for E. horridum are consistent with other attributes that are predicted for inselberg plants by the OCBIL theory, such as reduced dispersability and genetic isolation among populations. Those characteristics contribute to the isolation of E. horridum populations and heighten the importance of population-based conservation strategies for taxa that occur exclusively in those naturally fragmented inselbergs.
Additional keywords: Bromeliaceae, genetic diversity, plant evolution, plant breeding, pollination biology.
References
Aguiar LMS, Bernard E, Machado RB (2014) Habitat use and movements of Glossophaga soricina and Lonchophylla dekeyseri (Chiroptera: Phyllostomidae) in a neotropical savannah. Zoologia 31, 223–229.| Habitat use and movements of Glossophaga soricina and Lonchophylla dekeyseri (Chiroptera: Phyllostomidae) in a neotropical savannah.Crossref | GoogleScholarGoogle Scholar |
Ashman T-L, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421.
| Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences.Crossref | GoogleScholarGoogle Scholar |
Austerliz F, Smouse PE (2001) Two-Generation analysis of pollen flow across a landscape. II. Relation between Φft, pollen dispersal and inter female distance. Genetics 157, 851–857.
Barbará T, Martinelli G, Fay MF, Mayo SJ, Lexer C (2007) Population differentiation and species cohesion in two closely related plants adapted to neotropical high-altitude ‘inselbergs’, Alcantarea imperialis and Alcantarea geniculate (Bromeliaceae). Molecular Ecology 16, 1981–1992.
| Population differentiation and species cohesion in two closely related plants adapted to neotropical high-altitude ‘inselbergs’, Alcantarea imperialis and Alcantarea geniculate (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Barrett SCH (1998) The evolution of mating strategies in flowering plants. Trends in Plant Science 3, 335–341.
| The evolution of mating strategies in flowering plants.Crossref | GoogleScholarGoogle Scholar |
Bertin IE, Barnes C, Guttman SI (1989) Self-sterility and cryptic self-fertility in Campsis radicans (Bignoniaceae). Botanical Gazette 150, 397–403.
| Self-sterility and cryptic self-fertility in Campsis radicans (Bignoniaceae).Crossref | GoogleScholarGoogle Scholar |
BFG (2015) Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66, 1085–1113.
Borba EL, Semir J, Shepherd GJ (2001) Self-incompatibility, inbreeding depression and crossing potential in five Brazilian Pleurothallis (Orchidaceae) species. Annals of Botany 88, 89–99.
| Self-incompatibility, inbreeding depression and crossing potential in five Brazilian Pleurothallis (Orchidaceae) species.Crossref | GoogleScholarGoogle Scholar |
Bremer H, Sander H (2000) Inselbergs: geomorphology and geoecology. In ‘Ecological studies. Vol. 146: Inselbergs: biotic diversity of isolated rock outcrops in tropical and temperate regions’. (Eds S Porembski, W Barthlott) pp. 7–35. (Springer-Verlag: Berlin)
Burkle LA, Alarcón R (2011) The future of plant–pollinator diversity: understanding interaction networks across time, space, and global change. American Journal of Botany 98, 528–538.
| The future of plant–pollinator diversity: understanding interaction networks across time, space, and global change.Crossref | GoogleScholarGoogle Scholar |
Bustamante E, Búrquez A, Scheinvar E, Eguiarte LE (2016) Population genetic structure of a widespread bat-pollinated columnar cactus. PLoS One 11, e0152329
| Population genetic structure of a widespread bat-pollinated columnar cactus.Crossref | GoogleScholarGoogle Scholar |
Castellanos MC, Wilson P, Thomson JD (2003) Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57, 2742–2752.
| Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon.Crossref | GoogleScholarGoogle Scholar |
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nature Reviews. Genetics 10, 783–796.
| The genetics of inbreeding depression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1KrtbrI&md5=2dcd6e9b0b1a52e0f62c837a4b4ff640CAS |
Cheptou PO (2012) Clarifying Baker’s Law. Annals of Botany 109, 633–641.
| Clarifying Baker’s Law.Crossref | GoogleScholarGoogle Scholar |
Christianini AV, Forzza RC, Buzato S (2013) Divergence on floral traits and vertebrate pollinators of two endemic Encholirium bromeliads. Plant Biology 15, 360–368.
| Divergence on floral traits and vertebrate pollinators of two endemic Encholirium bromeliads.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38fntVOgug%3D%3D&md5=770a2342c093a85661361bd19e818d67CAS |
Cockerham CC (1969) Variance of gene frequencies. Evolution 23, 72–84.
| Variance of gene frequencies.Crossref | GoogleScholarGoogle Scholar |
Cosacov A, Nattero J, Cocucci AA (2008) Variation of pollinator assemblages and pollen limitation in a locally specialized system: the oil-producing Nierembergia linariifolia (Solanaceae). Annals of Botany 102, 723–734.
| Variation of pollinator assemblages and pollen limitation in a locally specialized system: the oil-producing Nierembergia linariifolia (Solanaceae).Crossref | GoogleScholarGoogle Scholar |
Dafni A, Kevan PG, Husband BC (2005) ‘Pratical pollination biology.’ (Enviroquest Ltd: Cambridge, ON, Canada)
Domingues R, Machado MA, Forzza RC, Melo TD, Wohlres-Viana S, Viccini LF (2011) Genetic variability of an endangered Bromeliaceae species (Pitcairnia albiflos) from the Brazilian Atlantic rainforest. Genetics and Molecular Research 10, 2482–2491.
| Genetic variability of an endangered Bromeliaceae species (Pitcairnia albiflos) from the Brazilian Atlantic rainforest.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbitlWnsQ%3D%3D&md5=54c76e618e241c7fa8a2a5cbb45bda41CAS |
Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou P, Goodwillie C, Johnston MO, Kelly JK, Moeller DA, Porcher E, Ree RH, Vallejo-Marín M, Winn AA (2010) Plant mating systems in a changing world. Trends in Ecology & Evolution 25, 35–43.
| Plant mating systems in a changing world.Crossref | GoogleScholarGoogle Scholar |
Faegri K, van der Pijl L (1979) ‘The principles of pollination biology.’ (Pergamon Press: Oxford, UK)
Ferrer MM, Good-Avila SV, Montaña C, Domínguez CA, Eguiarte LE (2009) Effect of variation in self-incompatibility on pollen limitation and inbreeding depression in Flourensia cernua (Asteraceae) scrubs of contrasting density. Annals of Botany 103, 1077–1089.
| Effect of variation in self-incompatibility on pollen limitation and inbreeding depression in Flourensia cernua (Asteraceae) scrubs of contrasting density.Crossref | GoogleScholarGoogle Scholar |
Fleming TH, Nunez RA, Sternberg LDSL (1993) Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis. Oecologia 94, 72–75.
| Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |
Fleming TH, Geiselman C, Kress WJ (2009) The evolution of bat pollination: a phylogenetic perspective. Annals of Botany 104, 1017–1043.
| The evolution of bat pollination: a phylogenetic perspective.Crossref | GoogleScholarGoogle Scholar |
Forzza RC (2005) Revisão taxonômica de Encholirium Mart. ex Schult. & Schult. F. (Pitcairnioideae – Bromeliaceae). Boletim de Botânica da Universidade de São Paulo 23, 1–49.
| Revisão taxonômica de Encholirium Mart. ex Schult. & Schult. F. (Pitcairnioideae – Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Forzza RC, Christianini AV, Wanderley MGL, Buzato S (2003) Encholirium (Pitcairnioideae - Bromeliaceae): conhecimento atual e sugestões para conservação. Vidalia 1, 7–20.
Forzza RC, Costa AF, Leme EMC, Versieux LM, Wanderley MGL, Louzada RB, Monteiro RF, Judice DM, Fernandez EP, Borges RAX, Penedo TSA, Monteiro NP, Moraes MA (2013) Bromeliaceae. In ‘Livro Vermelho da Flora do Brasil’. (Orgs G Martinelli, MA Moraes) pp. 315–390. (Andrea Jakobsson & Jardim Botânico do Rio de Janeiro: Rio de Janeiro)
Franklin-Tong VE (2008) ‘Self-incompatibility in flowering plants: evolution, diversity, and mechanisms.’ (Springer-Verlag: Berlin)
Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Functional Ecology 21, 434–443.
| The multifarious effects of dispersal and gene flow on contemporary adaptation.Crossref | GoogleScholarGoogle Scholar |
Geng Q, Ian CL, Goto S, Tao JI, Kimura M, Islam MDS, Hogetsu T (2008) Mating system, pollen and propagule dispersal, and spatial genetic structure in a high-density population of the mangrove tree Kandelia candel. Molecular Ecology 17, 4724–4739.
| Mating system, pollen and propagule dispersal, and spatial genetic structure in a high-density population of the mangrove tree Kandelia candel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCiurvM&md5=68035156e8f92ab3c91a68f1e152516bCAS |
Ghazoul J (2005) Pollen and seed dispersal among dispersed plants. Biological Reviews of the Cambridge Philosophical Society 80, 413–443.
| Pollen and seed dispersal among dispersed plants.Crossref | GoogleScholarGoogle Scholar |
Gibbs PE, Sassaki R (1998) Reproductive biology of Dalbergia miscolobium Benth. (Leguminosae-Papilionoideae) in SE Brazil: the effects of pistillate sorting on fruit-set. Annals of Botany 81, 735–740.
| Reproductive biology of Dalbergia miscolobium Benth. (Leguminosae-Papilionoideae) in SE Brazil: the effects of pistillate sorting on fruit-set.Crossref | GoogleScholarGoogle Scholar |
Gigord L, Lavigne C, Shykoff J (1998) Partial self-incompatibility and inbreeding depression in a native tree species of La Réunion (Indian Ocean). Oecologia 117, 342–352.
| Partial self-incompatibility and inbreeding depression in a native tree species of La Réunion (Indian Ocean).Crossref | GoogleScholarGoogle Scholar |
Gillet E, Hattemer HH (1989) Genetic analysis of isoenzyme phenotypes using single tree progenies. Heredity 63, 135–141.
| Genetic analysis of isoenzyme phenotypes using single tree progenies.Crossref | GoogleScholarGoogle Scholar |
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
| FSTAT (Version 1.2): a computer program to calculate F-statistics.Crossref | GoogleScholarGoogle Scholar |
Hao Y, Zhao X, She D, Xu B, Zhang D, Liao W (2012) The role of late-acting self-incompatibility and early-acting inbreeding depression in governing female fertility in monkshood, Aconitum kusnezoffii. PLoS One 7, e47034
| The role of late-acting self-incompatibility and early-acting inbreeding depression in governing female fertility in monkshood, Aconitum kusnezoffii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFKjt7%2FN&md5=d5c95bab09727550d9cbc256af2b1ba8CAS |
Hardy OJ, González-Martínez SC, Colas B, Fréville H, Mignot A, Olivieri I (2004) Fine-scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae). II. Correlated paternity within and among sibships. Genetics 168, 1601–1614.
| Fine-scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae). II. Correlated paternity within and among sibships.Crossref | GoogleScholarGoogle Scholar |
Hmeljevski KV, Reis A, Montagna T, Reis MS (2011) Genetic diversity, genetic drift and mixed mating system in small subpopulations of Dyckia ibiramensis, a rare endemic bromeliad from Southern Brazil. Conservation Genetics 12, 761–769.
| Genetic diversity, genetic drift and mixed mating system in small subpopulations of Dyckia ibiramensis, a rare endemic bromeliad from Southern Brazil.Crossref | GoogleScholarGoogle Scholar |
Hmeljevski KV, Ciampi MB, Baldauf C, Reis MS, Forzza RC (2013) Development of SSR markers for Encholirium horridum (Bromeliaceae) and transferability to other Pitcairnioideae. Applications in Plant Sciences 1, 1200445
| Development of SSR markers for Encholirium horridum (Bromeliaceae) and transferability to other Pitcairnioideae.Crossref | GoogleScholarGoogle Scholar |
Hmeljevski KV, Freitas L, Domingues R, Pereira AR, Cancio AS, Andrade ACS, Machado MA, Viccini LF, Forzza RC (2014) Conservation assessment of an extremely restricted bromeliad highlights the need for population-based conservation on granitic inselbergs of the Brazilian Atlantic Forest. Flora 209, 250–259.
| Conservation assessment of an extremely restricted bromeliad highlights the need for population-based conservation on granitic inselbergs of the Brazilian Atlantic Forest.Crossref | GoogleScholarGoogle Scholar |
Hmeljevski KV, Reis MS, Forzza RC (2015) Patterns of gene flow in Encholirium horridum L.B.Sm., a monocarpic species of Bromeliaceae from Brazil. The Journal of Heredity 106, 93–101.
| Patterns of gene flow in Encholirium horridum L.B.Sm., a monocarpic species of Bromeliaceae from Brazil.Crossref | GoogleScholarGoogle Scholar |
Hmeljevski KV, Nazareno AG, Bueno M, Reis MS, Forzza RC (2017) Do plant populations on distinct inselbergs talk to each other? A case study of genetic connectivity of a bromeliad species in an Ocbil landscape. Ecology and Evolution , in press.
Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically-buffered, infertile landscapes. Plant and Soil 322, 49–86.
| OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically-buffered, infertile landscapes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVWisrnN&md5=2e074035ab68170388a288068ec6cba1CAS |
Hopper SD, Silveira FAO, Fiedler PL (2016) Biodiversity hotspots and Ocbil theory. Plant and Soil 403, 167–216.
| Biodiversity hotspots and Ocbil theory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVKru7nI&md5=2445f67feca60bd33d355a14555adc41CAS |
Igic B, Lande R, Kohn JR (2008) Loss of self-incompatibility and its evolutionary consequences. International Journal of Plant Sciences 169, 93–104.
| Loss of self-incompatibility and its evolutionary consequences.Crossref | GoogleScholarGoogle Scholar |
Jacquemyn H, van Rossum F, Brys R, Endels P, Hermy M, Triest L, De Blust G (2003) Effects of agricultural land use and fragmentation on genetics, demography and population persistence of the rare Primula vulgaris, and implications for conservation. Belgian Journal of Botany 136, 5–22.
Karron JD, Holmquist KG, Flanagan RJ, Mitchell RJ (2009) Pollinator visitation patterns strongly influence among-flower variation in selfing rate. Annals of Botany 103, 1379–1383.
| Pollinator visitation patterns strongly influence among-flower variation in selfing rate.Crossref | GoogleScholarGoogle Scholar |
Kudo G (2006) Flowering phenologies of animal-pollinated plants: reproductive strategies and agents of selection. In ‘Ecology and evolution of flowers’. (Eds LD Harder, SCH Barrett) pp. 139–158. (Oxford University Press: New York)
Linhart YB (1973) Ecological and behavioural determinants of pollen dispersal in hummingbird- pollinated Heliconia. American Naturalist 107, 511–523.
| Ecological and behavioural determinants of pollen dispersal in hummingbird- pollinated Heliconia.Crossref | GoogleScholarGoogle Scholar |
Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15, 65–95.
| Ecological determinants of genetic structure in plant populations.Crossref | GoogleScholarGoogle Scholar |
Lüttge U (2008) ‘Physiological ecology of tropical plants.’ (Springer-Verlag: Berlin)
MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. American Naturalist 100, 603–609.
| On optimal use of a patchy environment.Crossref | GoogleScholarGoogle Scholar |
Maguire JD (1962) Speed of germination – aid in selection and evaluation for seedling emergence and vigor. Crop Science 2, 176–177.
| Speed of germination – aid in selection and evaluation for seedling emergence and vigor.Crossref | GoogleScholarGoogle Scholar |
Martin FN (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Technology 34, 125–128.
| Staining and observing pollen tubes in the style by means of fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG1M%2FovV2jtQ%3D%3D&md5=4165cdb07b9876dd5b239b294799f757CAS |
Matallana G, Godinho MAS, Guilherme FAG, Belisario M, Coser TS, Wendt T (2010) Breeding systems of Bromeliaceae species: evolution of selfing in the context of sympatric occurrence. Plant Systematics and Evolution 289, 57–65.
| Breeding systems of Bromeliaceae species: evolution of selfing in the context of sympatric occurrence.Crossref | GoogleScholarGoogle Scholar |
Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD (2009) Ecology and evolution of plant–pollinator interactions. Annals of Botany 103, 1355–1363.
| Ecology and evolution of plant–pollinator interactions.Crossref | GoogleScholarGoogle Scholar |
Muchhala N, Caiza A, Vizuete JC, Thomson JD (2009) A generalized pollination system in the tropics: bats, birds and Aphelandra acanthus. Annals of Botany 103, 1481–1487.
| A generalized pollination system in the tropics: bats, birds and Aphelandra acanthus.Crossref | GoogleScholarGoogle Scholar |
Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution 15, 278–285.
| Spatial patterns of seed dispersal, their determinants and consequences for recruitment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbitlOqtA%3D%3D&md5=253262f15fd1646c4be47ab7d7571b2aCAS |
Nistelberger HM, Byrne M, Coates D, Roberts JD (2015) Genetic drift drives evolution in the bird-pollinated, terrestrial island endemic Grevillea georgeana (Proteaceae). Botanical Journal of the Linnean Society 178, 155–168.
| Genetic drift drives evolution in the bird-pollinated, terrestrial island endemic Grevillea georgeana (Proteaceae).Crossref | GoogleScholarGoogle Scholar |
Ohashi K, Thomson JD (2009) Trapline foraging by pollinators: its ontogeny, economics and possible consequences for plants. Annals of Botany 103, 1365–1378.
| Trapline foraging by pollinators: its ontogeny, economics and possible consequences for plants.Crossref | GoogleScholarGoogle Scholar |
Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56, 717–728.
| Multiple meanings and modes: on the many ways to be a generalist flower.Crossref | GoogleScholarGoogle Scholar |
Osborne JL, Clark SJ, Morris RJ, Williams IH, Riley JR, Smith AD, Reynolds DR, Edwards AS (1999) A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. Journal of Applied Ecology 36, 519–533.
| A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar.Crossref | GoogleScholarGoogle Scholar |
Pannell JR, Fields PD (2014) Evolution in subdivided plant populations: concepts, recent advances and future directions. New Phytologist 201, 417–432.
| Evolution in subdivided plant populations: concepts, recent advances and future directions.Crossref | GoogleScholarGoogle Scholar |
Pasquet RS, Peltier A, Hufford MB, Oudin E, Saulnier J, Paul L, Knudsen JT, Herren HR, Gepts P (2008) Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proceedings of the National Academy of Sciences of the United States of America 105, 13456–13461.
| Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFChs7rE&md5=bb74419552fd690e9bca1d3b51c9dbeeCAS |
Phillips RD, Hopper SD, Dixon KW (2010) Pollination ecology and the possible impacts of environmental change in the southwest Australian biodiversity hotspot. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365, 517–528.
| Pollination ecology and the possible impacts of environmental change in the southwest Australian biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |
Porembski S (2007) Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Brazilian Journal of Botany 30, 579–586.
| Tropical inselbergs: habitat types, adaptive strategies and diversity patterns.Crossref | GoogleScholarGoogle Scholar |
Porembski S, Barthlott W (2000) Inselbergs. In ‘Biotic diversity of isolated rock outcrops in tropical and temperate regions’. (Springer-Verlag: Berlin)
Queiroz JA, Quirino ZGM, Machado IC (2015) Floral traits driving reproductive isolation of two co-flowering taxa that share vertebrate pollinators. AoB Plants 7, plv127
| Floral traits driving reproductive isolation of two co-flowering taxa that share vertebrate pollinators.Crossref | GoogleScholarGoogle Scholar |
Ritland K (1989) Correlated matings in the partial selfer Mimulus guttatus. Evolution 43, 848–859.
| Correlated matings in the partial selfer Mimulus guttatus.Crossref | GoogleScholarGoogle Scholar |
Ritland K (2009) ‘Multilocus mating system program MLTR ver. 3.4.’ (University of British Columbia: Vancouver) Available at http://genetics.forestry.ubc.ca/ritland/programs.html [Verified 3 May 2017].
Rothenwöhrer C, Becker NI, Tschapka M (2011) Resource landscape and spatio-temporal activity patterns of a plant visiting bat in a Costa Rica lowland rainforest. Journal of Zoology 283, 108–116.
| Resource landscape and spatio-temporal activity patterns of a plant visiting bat in a Costa Rica lowland rainforest.Crossref | GoogleScholarGoogle Scholar |
Safford H, Martinelli G (2000) Inselbergs: geomorphology and geoecology. In ‘Biotic diversity of isolated rock outcrops in tropical and temperate regions’. (Eds S Porembski, W Barthlott) pp. 339–385. (Springer-Verlag: Berlin)
Sánchez-Lafuente AM, Guitián J, Medrano M, Herrera CM, Rey PJ, Cerdá X (2005) Plant traits, environmental factors, and pollinator visitation in winter-flowering Helleborus foetidus (Ranunculaceae). Annals of Botany 96, 845–852.
| Plant traits, environmental factors, and pollinator visitation in winter-flowering Helleborus foetidus (Ranunculaceae).Crossref | GoogleScholarGoogle Scholar |
Sazima I, Vogel S, Sazima M (1989) Bat pollination of Encholirium glaziovii, a terrestrial bromeliad. Plant Systematics and Evolution 168, 167–179.
| Bat pollination of Encholirium glaziovii, a terrestrial bromeliad.Crossref | GoogleScholarGoogle Scholar |
Schurr FM, Bond WJ, Midgley GF, Higgins SI (2005) A mechanistic model for secondary seed dispersal by wind and its experimental validation. Journal of Ecology 93, 1017–1028.
| A mechanistic model for secondary seed dispersal by wind and its experimental validation.Crossref | GoogleScholarGoogle Scholar |
Seavey SR, Bawa KS (1986) Late-acting self-incompatibility. Botanical Review 52, 195–219.
| Late-acting self-incompatibility.Crossref | GoogleScholarGoogle Scholar |
Silveira FAO, Negreiros D, Barbosa NPU, Buisson E, Carmo FF, Carstensen DW, Conceição AA, Cornelissen TG, Echternacht L, Fernandes GW, Garcia QS, Guerra TJ, Jacobi CM, Lemos-Filho JP, Le Stradic S, Morellato LPC, Neves FS, Oliveira RS, Schaefer CE, Viana PL, Lambers H (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant and Soil 403, 129–152.
| Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlCqtL7P&md5=9709bd6a52771b7d86fcc5f3ea6f1318CAS |
Smouse PE, Dyer RJ, Westfall D, Sork VL (2001) Two-generation analysis of pollen flow across a landscape. I. Male gamete heterogeneity among females. Evolution 55, 260–271.
| Two-generation analysis of pollen flow across a landscape. I. Male gamete heterogeneity among females.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFOksr0%3D&md5=6145440d0851bad04bcffd7304d41103CAS |
StatSoft Inc. (2004) ‘STATISTICA (data analysis software system) ver. 7.’ Available at http://www.statsoft.com [Verified 3 May 2017].
Szarzynski J (2000) Xeric islands: environmental conditions in inselbergs. In ‘Biotic diversity of isolated rock outcrops in tropical and temperate regions’. (Eds S Porembski, W Barthlott) pp. 37–48. (Springer-Verlag: Berlin)
Tapper S-L, Byrne M, Yates CJ, Keppel G, Hopper SD, Van Niel K, Schut AGT, Mucina L, Wardell-Johnson GW (2014) Isolated with persistence or dynamically connected? Genetic patterns in a common granite outcrop endemic. Diversity & Distributions 20, 987–1001.
| Isolated with persistence or dynamically connected? Genetic patterns in a common granite outcrop endemic.Crossref | GoogleScholarGoogle Scholar |
Traveset A, Rodríguez-Pérez J, Pías B (2008) Seed trait changes in dispersers’ guts and consequences for germination and seedling growth. Ecology 89, 95–106.
| Seed trait changes in dispersers’ guts and consequences for germination and seedling growth.Crossref | GoogleScholarGoogle Scholar |
Valido A, Dupont YL, Hansen DM (2002) Native birds and insects, and introduced honey bees visiting Echium wildpretii (Boraginaceae) in the Canary Islands. Acta Oecologica 23, 413–419.
| Native birds and insects, and introduced honey bees visiting Echium wildpretii (Boraginaceae) in the Canary Islands.Crossref | GoogleScholarGoogle Scholar |
Vallejo-Marín M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annual Review of Ecology Evolution and Systematics 41, 193–213.
| The ecological and evolutionary consequences of clonality for plant mating.Crossref | GoogleScholarGoogle Scholar |
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
| Micro-checker: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=288416d6dcd7f33872c36fce13a9cce5CAS |
von Helversen O, Reyer HU (1984) Nectar intake and energy expenditure in a flower visiting bat. Oecologia 63, 178–184.
| Nectar intake and energy expenditure in a flower visiting bat.Crossref | GoogleScholarGoogle Scholar |
Vosgueritchian SB, Buzato S (2006) Reprodução sexuada de Dyckia tuberosa (Vell.) Beer (Bromeliaceae, Pitcairnioideae) e interação planta-animal. Revista Brasileira de Botanica. Brazilian Journal of Botany 29, 433–442.
| Reprodução sexuada de Dyckia tuberosa (Vell.) Beer (Bromeliaceae, Pitcairnioideae) e interação planta-animal.Crossref | GoogleScholarGoogle Scholar |
Waser NW, Chittka L, Price MV, Willians NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77, 1043–1060.
| Generalization in pollination systems, and why it matters.Crossref | GoogleScholarGoogle Scholar |
Wolowski M, Freitas L (2015) An overview on pollination of the neotropical Poales. Rodriguésia 66, 329–336.
| An overview on pollination of the neotropical Poales.Crossref | GoogleScholarGoogle Scholar |
Wolowski M, Ashman T-L, Freitas L (2014) Meta-analysis of pollen limitation reveals the relevance of pollination generalization in the Atlantic forest of Brazil. PLoS One 9, e89498
| Meta-analysis of pollen limitation reveals the relevance of pollination generalization in the Atlantic forest of Brazil.Crossref | GoogleScholarGoogle Scholar |
Wolowski M, Carvalheiro LG, Freitas L (2017) Influence of plant–pollinator interactions on the assembly of plant and hummingbird communities. Journal of Ecology 105, 332–344.
| Influence of plant–pollinator interactions on the assembly of plant and hummingbird communities.Crossref | GoogleScholarGoogle Scholar |
Yates CJ, Ladd PG, Coates DJ, McArthur S (2007) Hierarchies of cause: understanding rarity in an endemic shrub Verticordia staminosa (Myrtaceae) with a highly restricted distribution. Australian Journal of Botany 55, 194–205.
| Hierarchies of cause: understanding rarity in an endemic shrub Verticordia staminosa (Myrtaceae) with a highly restricted distribution.Crossref | GoogleScholarGoogle Scholar |
Zapata TR, Arroyo MTK (1978) Plant reproductive ecology of a secondary deciduous tropical Forest in Venezuela. Biotropica 10, 221–230.
| Plant reproductive ecology of a secondary deciduous tropical Forest in Venezuela.Crossref | GoogleScholarGoogle Scholar |
